Mosquitoes (Diptera: Culicidae) in : a review of their biodiversity, distribution and medical importance Aichetou Mint Mohamed Lemine, Mohamed Aly Ould Lemrabott, Moina Hasni Ebou, Khadijetoumint Lekweiry, Mohamed Salem Ould Ahmedou Salem, Khyarhoum Ould Brahim, Mohamed Ouldabdallahi Moukah, Issa Nabiyoullahi Ould Bouraya, Cecile Brengues, Jean-Francois Trape, et al.

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Aichetou Mint Mohamed Lemine, Mohamed Aly Ould Lemrabott, Moina Hasni Ebou, Khadijetoumint Lekweiry, Mohamed Salem Ould Ahmedou Salem, et al.. Mosquitoes (Diptera: Culicidae) in Mau- ritania: a review of their biodiversity, distribution and medical importance. Parasites and Vectors, BioMed Central, 2017, 10 (1), ￿10.1186/s13071-017-1978-y￿. ￿hal-01521348￿

HAL Id: hal-01521348 https://hal.archives-ouvertes.fr/hal-01521348 Submitted on 7 May 2018

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Mint Mohamed Lemine et al. Parasites & Vectors (2017) 10:35 DOI 10.1186/s13071-017-1978-y

REVIEW Open Access Mosquitoes (Diptera: Culicidae) in Mauritania: a review of their biodiversity, distribution and medical importance Aichetou Mint Mohamed Lemine1,2, Mohamed Aly Ould Lemrabott1, Moina Hasni Ebou1,KhadijetouMintLekweiry1, Mohamed Salem Ould Ahmedou Salem1, Khyarhoum Ould Brahim1, Mohamed Ouldabdallahi Moukah1, Issa Nabiyoullahi Ould Bouraya3,CecileBrengues4, Jean-François Trape4, Leonardo Basco5, Hervé Bogreau5,6, Frédéric Simard4, Ousmane Faye2 and Ali Ould Mohamed Salem Boukhary1*

Abstract Although mosquitoes (Diptera: Culicidae) are important disease vectors, information on their biodiversity in Mauritania is scarce and very dispersed in the literature. Data from the scientific literature gathered in the country from 1948 to 2016 were collected and analyzed. Overall 51 culicid species comprising 17 Anopheles spp., 14 Aedes spp., 18 Culex spp. and two Mansonia spp. have been described in Mauritania among which Anopheles arabiensis, Aedes vexans, Culex poicilipes and Culex antennatus are of epidemiological significance. Anopheles arabiensis is widely distributed throughout the country and its geographic distribution has increased northwards in recent years, shifting its northern limit form 17°32′N in the 1960s to 18°47′N today. Its presence in the central region of Tagant highlights the great ecological plasticity of the species. Conversely, the distribution of Anopheles gambiae (s.s.) and Anopheles melas has shrunk compared to that of the 1960s. Anopheles rhodesiensis and An. d’thali are mainly confined in the mountainous areas (alt. 200–700 m), whereas Anopheles pharoensis is widely distributed in the River basin. Culex poicilipes and Cx. antenattus were naturally found infected with Rift valley fever virus in central and northern Mauritania following the Rift valley outbreaks of 1998 and 2012. Recently, Ae. aegypti emerged in and is probably responsible for dengue fever episodes of 2015. This paper provides a concise and up-to-date overview of the existing literature on mosquito species known to occur in Mauritania and highlights areas where future studies should fill a gap in knowledge about vector biodiversity. It aims to help ongoing and future research on mosquitoes particularly in the field of medical entomology to inform evidence-based decision-making for vector control and management strategies. Keywords: Culicidae, Biodiversity, Mosquitoes, Vector, Rift Valley fever, Dengue, Malaria, Mauritania

Background and YF are acute febrile mosquito-borne viral diseases of Mosquitoes (Diptera: Culicidae) are considered one of man and animals (RVF) which cause clinical syndromes the most relevant groups of arthropods in public health ranging from an uncomplicated form with fever to [1, 2]. Those belonging to the genera Aedes, Anopheles hemorrhagic disease in humans and abortions and and Culex are of interest because of their role in the mortality during epizootics in livestock [3]. Malaria, the transmission of a variety of human and animal diseases deadliest vector-borne parasitic disease worldwide, is such as Rift Valley fever (RVF), dengue fever (DF), yel- caused by a protozoan belonging to the genus Plasmo- low fever (YF), Zika, chikungunya and malaria. RVF, DF dium. According to the World Health Organization (WHO), vector-borne diseases account for 17% of the * Correspondence: [email protected] estimated global burden of all infectious diseases mostly 1Unité de recherche Génomes et Milieux, Jeune Equipe Associée à l’IRD due to malaria and DF [4]. (RI3M), Université de Nouakchott Al-Aasriya, Faculté des Sciences et Techniques, Nouveau Campus Universitaire, Nouakchott BP 5026, Mauritania Mosquitoes are dipterans of the suborder Nematocera, Full list of author information is available at the end of the article all placed within the family Culicidae. Approximately

© The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Mint Mohamed Lemine et al. Parasites & Vectors (2017) 10:35 Page 2 of 13

3500 species and subspecies in 44 genera are recognized of inhabitants) in the southern Sahelian region and along globally [5]. The cosmopolitan genera Anopheles with the . Settlement of nomad populations and seven subgenera involving 460 recognized species, Culex rural exodus, partly related to the periods of drought in the with 26 subgenera comprising 763 species and the Old 1970s, 1980s and 1990s, are the most significant demo- World and Nearctic genus Aedes with 70 subgenera in- graphic phenomena that have occurred in Mauritania since cluding 927 species are the highest in species diversity the country’s independence in 1960. Whereas the propor- and most important for public health in the family [5, 6]. tion of urban population was 9% in 1965, it increased to Historically, five large outbreaks of RVF occurred in 22.7, 46.7 and 60% in 1977, 2005 and 2010, respectively. Mauritania in 1987, 1998, 2003, 2010 and 2012 resulting Over the same period, the nomad population rapidly in a high number of human fatalities and major losses in decreased from 65% in 1965 to 12, 6 and 2% in 1988, the livestock population [7–12]. Furthermore, the WHO 2000 and 2013, respectively [25]. Mauritania has a large outbreaks and emergencies bulletin reported DF and livestock population with 1,247,000 camels, 1,657,000 RVF events in Mauritania in 2015 [13]. Although in this cattle, 12,555,000 small ruminants (sheep and goats) bulletin, the areas in which these outbreaks have oc- and an important population of equines (donkeys and curred were not specified, data from the Mauritanian horses) estimated at 212,000 [26]. The livestock dens- Ministry of Health have cited Nouakchott, the capital ity is higher in southern Mauritania compared to that city and the southern for DF and RVF, re- of its arid northern part. spectively (Ouldabdallahi Moukah, pers. comm.). Despite being largely arid, there are several temporary Moreover, malaria is endemic in the southern regions and permanent wetland areas in Mauritania. The most of the country and in parts of the Saharan region, in- important are the Senegal River Delta, the protected cluding Nouakchott, the capital city, where peak trans- coastal Banc d’Arguin National Park and the Diawling mission occurs in September and October during and National Park, the natural lakes of , Mal, Rkiz, mare shortly after the rainy season [14–17]. Approximately, de Kankoussa, mare de Mahmoude and more than 300 two-thirds of the resident population of Mauritania is oases [27, 28]. exposed to the risk of malaria. Mauritania is an arid country with two-thirds of its sur- In Mauritania, knowledge about the Culicidae fauna face area lying within the arid zone of the Saharan desert has been closely related to studies on human health, like (0–100 mm annual rainfall) and the remainder belongs to the malariometric surveys of 1942 during the colonial the Sahelian zone (100–500 mm annual rainfall). period [18] and those of 1960s to assess malaria epi- Rain is relatively scarce and irregular over the country. demiology [19–21] and more recently after the recurrent It falls between July and September, with an increased RVF outbreaks [9, 12, 22, 23]. It is worth noting that gradient from North to South, ranging from less than there are no published data on mosquitoes in the coun- 50 mm annually in the northern Saharan zone to 500 mm try for the period 1970–1990 probably because of the in parts of the southernmost region of Guidimagha (Fig. 2). prolonged period of drought in the 1970s and 1980s in Studies on the variability of rainfall in Mauritania showed a the Sahel [24] during which food security had become a significant decreasing trend in annual rainfall because of priority over public health in most Sahelian countries. prolonged drought of 1970–1990. For instance, in the Although mosquitoes are important disease vectors, Sahelian southern part of the country, average rainfall de- information on mosquito biodiversity in Mauritania is creased by 120 mm (39%) between the periods 1933–1969 scarce and notably dispersed in the literature. Therefore, (310 mm) and 1970–1999 (190 mm) [29] which resulted in there is an urgent need for more detailed understanding a southward movement of 250 and 500 mm rainfall isohy- of the biodiversity, distribution and ecology of mosquito etal lines as reported by Mahé et al. [30] (Fig. 2). However, species known to occur in the country. This paper pro- it is not yet clear whether the unusual heavy rainfalls that vides the first comprehensive review on mosquitoes in occurred in the last decade, particularly in 2003, 2006, 2010 Mauritania and analyses data collected from the scien- and 2013, are signs of the establishment of sustainable wet- tific literature and published reports available within the ter conditions as suggested by De Longueville et al. [31]. country. Mean annual temperatures over the country range from 20 °C in January to 33.7 °C in June. According to Salient data on Mauritania McSweeney et al. [32], the mean annual temperature in Mauritania (15°–27° N latitude and 5°–17° W longitude) Mauritania has increased by 0.9 °C since 1960, with an is in northwest Africa at the intersection of the Maghreb average rate of 0.19 °C per decade. region and sub-Saharan West Africa (Fig. 1). It covers an area of 1,030,700 km2, and has a population of Culicidae fauna in Mauritania 3,378,250, and a mean population density of 3.3 persons/ Overall, 51 mosquito species belonging to four genera km2. The population is predominantly distributed (i.e. 80% were described in Mauritania between 1948 and 2016 Mint Mohamed Lemine et al. Parasites & Vectors (2017) 10:35 Page 3 of 13

Fig. 1 Map of Mauritania with its administrative regions. Administrative district codes are provided in parentheses

(Table 1). Published literature before 1970 mentioned 41 been prospected) during the dry season between November mosquito species comprising 13 Anopheles spp., 9 Aedes 1962 and March 1963 and shortly after the wet sea- spp., 17 Culex spp. and 2 Mansonia spp., while from son (October and November) in 1963. Their investiga- 2000 until now 34 mosquito species, involving 15 tions were not only focused on Anopheles mosquitoes but Anopheles spp., 8 Aedes spp., 9 Culex spp. and 2 Manso- also considered other arthropods of medical importance. nia spp., were described. The distribution of mosquitoes They reported the presence of the following 12 Anopheles of medical importance in Mauritania is given in Fig. 3. species and subspecies in the prospected zones: An. funes- tus, An. gambiae (sensu lato)(s.l.), An. pharoensis, An. Anopheles spp. rufipes, An. melas, An. d’thali, An. rhodesiensis, An. cous- Until 1960, only six species of Anopheles were known to tani, An. ziemmani, An. pretoriensis, An. squamosus and occur in Mauritania namely An. gambiae, An. melas, An. demeilloni. Among these, An. gambiae (s.l.)andAn. An. funestus, An. pharoensis, An. rufipes and An. d’thali funestus are the major malaria vectors in Africa. Entomo- [18, 33, 34]. In a malariometric survey conducted during logical survey conducted by Pichon & Ouedraogo [35] the dry season extending from December 1962 to April aiming at the search of areas fulfilling the conditions for 1963, Maffi [19] searched for Anopheles larvae in a limited the emergence of yellow fever epidemics confirmed the number of breeding sites in southern Mauritania (Tagant, findings of Hamon et al. [20, 21]. Coz [36] in his work Brakna, Gorgol, Trarza, Assaba and Hodh Elgharbi). The conducted in the late of 1960s in southeastern Mauritania, author confirmed the presence of An. gambiae, An. phar- reported the presence of only An. gambiae (species A), oensis, An. d’thali and An. rufipes larvae in the breeding later known as Anopheles gambiae (s.s.)infivesites,in- sites and showed the presence of An. rhodesiensis. cluding the very dry area of (17°32′N) belong- This work was followed by a more comprehensive ing to the . The author considered the work by Hamon et al. [20, 21]. These authors conducted presence of An. gambiae (s.s.) in the very dry areas of extensive surveys to assess malaria endemicity in Adrar, Mauritania difficult to explain but conjectured that relict Assaba, Trarza, Gorgol and Hodh Elgharbi regions populations of this species may have remained after wider (Guidimagha, the wettest region of Mauritania had not distribution of this species before desertification. Mint Mohamed Lemine et al. Parasites & Vectors (2017) 10:35 Page 4 of 13

Fig. 2 Rainfall isohyets for 1940–1999 in Mauritania. Insert: 250 and 500 mm isohyetal line shifts for the humid period of 1940–1969 (dotted lines) and the dry period of 1970–1999 (continuous lines). (Adapted from Mahé et al. [30])

During the survey conducted in 1984 by Baudon et al. traps, from five localities in the Hodh Elgharbi southeast- [37] at the Foum gleita Dam in the during ern region of Mauritania following the RVF outbreak of the dry season, no anopheline was caught, although in the 1998. Anopheles rhodesiensis was also reported in two same period, specimens of An. gambiae (s.s.), An. arabien- localities of the northern Adrar and the central Tagant sis and An. melas, were captured in several Senegalese lo- [42, 43]. However, Trape [44] re- calities on the other side of the Senegal river valley [38]. ported only An. d’thali in 8 of 13 localities prospected in In 1996 and 1997, Molez & Faye [39] studied a south- the and An. pharoensis, An. d’thali and An. north transect from Boghé on the Senegal River (middle arabiensis in the during the dry season of Delta) to Rachid (18°47′N), in the stony desert plateau of 2004. During the RVF outbreak of 2003, an entomological Tagant region. They noted the similitude in the compos- survey covering Trarza, Brakna, Assaba, Tagant and ition of the mosquito fauna between northern Senegal and Hodh Elgharbi regions was conducted in October and southern Mauritania along the Senegal River with An. ara- November of the same year [22]. Among 647 anopheline biensis found throughout the transect and An. rhodesiensis specimens collected using pyrethrum space-spray catch captured only in the Tagant region. Anopheles flavicosta (PSC) method, An. gambiae M form, now known as An. was also reported in Mauritania, but the location where it coluzzii [45] and An. arabiensis, both members of the An. was found was not specified [40]. More recently, Nabeth gambiae (s.l.) complex, represented 92% of the specimens, et al. [41] collected An. pharoensis, An. rhodesiensis and followed by An. pharoensis (5%) and An. funestus (3%). An. rufipes using Centers for Disease Control (CDC)-light Specimens of An. funestus were observed only in Brakna Mint Mohamed Lemine et al. Parasites & Vectors (2017) 10:35 Page 5 of 13

Table 1 List of the Culicidae species collected as adult (A) and larva (L), and their distribution in Mauritania Genus Species (development stage) Distributiona References Before 1970 Recent (2000-present) Anopheles spp. An. arabiensis (A, L) An. arabiensis (A, L) Brk, Hch, Hgh, Gmg, Nkc, Tag, Trz [8, 20, 22, 42, 43, 47, 48] An. coustani (A, L) An. coustani (A) Asb, Brk, Grg, Hgh, Trz [8, 20, 35] An. demeilloni (A, L) Hgh [20] An. d’thali (A, L) An. d’thali (A, L) Adr, Hgh, Tag [19, 20, 34, 44] An. domicola (A) Gdm, Grg [48] An. flavicosta na [40] An. freetownensis (A) Hgh [8] An. funestus (A, L) An. funestus (A Asb, Brk, Grg, Gmg; Hgh, Tag, Trz [8, 9, 18, 20, 22, 23, 35, 47] An. gambiae (A, L) An. gambiae (A, L) Asb, Brk, Grg, Hch, Hgh, Trz [9, 18, 22, 35, 36, 42, 43, 47, 48] An. melas (A) Trz [20, 33] An. pharoensis (A, L) An. pharoensis (A, L) Adr, Asb, Brk, Grg, Hgh, Trz, Tag [8, 9, 18, 20, 22, 23, 35, 41–44, 47, 48] An. pretoriensis (L) An. pretoriensis (A Hgh [8, 12, 20] An. rhodesiensis (A, L) An. rhodesiensis (A, L) Adr, Asb, Hgh, Tag [8, 19, 20, 23, 41–43, 48] An. rufipes (A, L) An. rufipes (A, L) Asb, Brk, Grg, Hgh, Tag, Trz [8, 9, 18, 20, 23, 35, 41–43, 47, 48] An. squamosus (A, L) An. squamosus (A) Adr, Asb, Brk, Grg, Hgh, Trz [8, 9, 20] An. wellcomei (A) na [9] An. ziemanni (A, L) An. ziemanni (A Brk, Hgh, Tag [8, 9, 20, 23, 42, 48] Aedes spp. Ae. aegypti (A, L) Ae. aegypti (A, L) Hch, Gmg, Grg, Nkc [35, 51, 54, 55] Ae. caspius (A, L) Nkc [51] Ae. vexans (A) Ae. vexans (A, L) Adr, Asb, Grg, Hgh, Tag, Trz [8–10, 21, 23, 43, 57] Ae. dalzieli (A) Hgh [8] Ae. fowleri (A) Hgh [8] Ae. minutus (A) Hgh [8] Ae. sudanensis (A) Tag [23] Ae. vittatus (A, L) Gmg, Grg, Hgh [35, 54, 55] Ae. luteocephalus (A) Grg [21] Ae. scatophagoides (A) Grg, Gmg [21, 35] Ae. metallicus (A) Grg [21] Ae. ochraceus (A) Ae. ochraceus (A) Grg, Hgh [8, 9, 21] Ae. hirsutus (A) Hgh [35] Ae. argenteopunctatus (A) Hch [35] Culex spp. Cx. antennatus (A, L) Cx. antennatus (A) Adr, Brk, Grg, Hgh, Tag, Trz [8, 9, 21, 23, 35, 41] Cx. poicilipes (A, L) Cx. poicilipes (A) Asb, Brk, Grg, Hgh, Tag, Trz [8, 9, 21, 23, 35, 41] Cx. ethiopicus (A, L) Cx. ethiopicus (A) Asb, Brk, Grg, Hgh, Tag [8, 9, 21, 35] Cx. quinquefasciatus (A) Dkh, Ich, Tir, Trz, Tag, [8, 23, 41, 43] Cx. duttoni (L) Gmg, Hgh [35] Cx. grahami (L) Brk, Hgh [35] Cx. annulioris (L) Hgh [35] Cx. univittatus (A, L) Adr, Asb, Brk, Grg, Hgh, Tag, Trz [21, 35] Cx. simpsoni (L) Grg, Hgh [21, 35] Cx. pipiens (A, L) Adr, Hgh [21, 35] Cx. nebulosus (A, L) Gmg [35] Cx. fatigans (A, L) Grg, Nkc, Trz [21, 35] Mint Mohamed Lemine et al. Parasites & Vectors (2017) 10:35 Page 6 of 13

Table 1 List of the Culicidae species collected as adult (A) and larva (L), and their distribution in Mauritania (Continued) Cx. decens (A, L) Cx. decens (A) Adr, Asb, Hgh, Tag, [8, 21, 23, 35, 41] Cx. perfuscus (A) Cx. perfuscus (A) Adr, Asb, Hgh [8, 21, 35, 41] Cx. neavei (A) Cx. neavei (A) Adr, Hgh, Tag [8, 9, 23, 35] Cx. perexiguus (A, L) Adr, Asb, Hgh, Grg, Nkc, Tag, Trz [21] Cx. tritaeniorhynchus (L) Cx. tritaeniorhynchus (A) Adr, Brk, Trz [9, 35] Cx. tigripes (A, L) Cx. tigripes (A) Asb, Grg, Hgh, Trz [21, 35] Mansonia spp. Ma. uniformis (A) Ma. uniformis (A) Adr, Brk, Grg, Hgh, Tag, Trz [9, 10, 21, 23, 35] Ma. africana (A) Ma. africana (A) Gmg, Grg [9, 21, 35] Abbreviations: Adr Adrar, Asb Assaba, Brk Brakna, Dkh Dakhlet , Gdm Guidimagha, Grg Gorgol, Hch Hodh Charghi, Hgh Hodh Elgharbi, Ich Inchiri, Nkc Nouakchott, Tag Tagant, Tir Tiris Zemmour, Trz Trarza, na not avaliable aDistrict codes are as in Fig. 1

Fig. 3 Distribution of mosquitoes of medical importance in Mauritania with indication of the northern limit of An. arabiensis (dotted line). 1, An arabiensis;2,An. gambiae (s.s.); 3, An. funestus;4,An. melas;5,An. pharoensis;6,An. ziemanni;7,An. wellcomei;8,Aedes aegypti;9,Ae. vexans; 10, Culex poicilipes; 11, Cx. antenattus Mint Mohamed Lemine et al. Parasites & Vectors (2017) 10:35 Page 7 of 13

region adjacent to the Senegal River basin. In all pros- with or without vegetation and organic debris. Its pres- pected areas An. gambiae (s.l.) showed no significant dif- ence was noted in Tagant, Assaba and Adrar region [19]. ference in their anthropophilic rates and all An. funestus Anopheles d’thali larvae were present in all surface water and An. pharoensis specimens had fed on human and of the Adrar region, even in those that are highly brack- ovine hosts, respectively. Furthermore, of 394 females of ish. They were particularly abundant when the deposits the An. gambiae complex tested in Assaba, one An. ara- contained filamentous green algae, on which eggs were biensis was positive for P. falciparum circumsporozoite abundant. In Hodh Elgharbi and Tagant, the larvae were antigen, giving an infection rate of 0.25% in this region found in fresh water sources with abundant aquatic and 0.17% in the whole study area. During the same RVF vegetation and organic debris, and in residual spill of outbreak of 2003, Faye et al. [9] further reported the pres- Gueltas (i.e. large rocky basin filled with water) without ence of An. rufipes, An. wellcomei, An. ziemanni and An. vegetation [20]. Anopheles coustani var. ziemanni larvae squamosus, in Trarza, Brakna and Assaba southern re- were collected in grassy swamps, ponds with Pistia stra- gions but the authors did not describe the localities where tiofes and streams with abundant vegetation. Water at the mosquitoes were captured since their investigations breeding sites was sometimes very slightly brackish [20]. were focused on the potential vectors of RVF. It is worth Anopheles funestus larvae were found in a large perman- noting that in an entomological survey conducted follow- ent pond with Pistia and slightly brackish water [20]. ing the RVF outbreak of 2012 five anopheline species in- Anopheles demeilloni larvae were encountered in a cluding An. funestus, An. pharoensis, An. rhodesiensis, An. stream from a permanent source with abundant vegeta- rufipes and An. ziemanni were captured in and tion and organic debris. Anopheles gambiae (s.s.) larvae in the central region of Tagant, and Tamcheket in were captured in a variety of breeding sites with some- the southeastern region of Hodh Elgharbi [23]. times slightly brackish water including residual puddles Using the PSC method to collect indoor resting mos- of ponds and rivers, ponds with or without silt and quitoes in Nouakchott (Saharan zone) and Hodh Tamourts (i.e. temporary pond of sub-desertic areas Elgharbi (Sahelian zone), Mint Lekweiry et al. [46, 47] densely shaded by huge Acacia, streams near their ori- reported that An. arabiensis is the sole anopheline spe- gin), Oglas (i.e. shallow hole to reach ground water in cies in Nouakchott and showed the infection of three of the beds of temporary wadis), overflow areas of the 186 specimens (1.6%) with P. vivax circumsporozoite Senegal River constituting flooded meadows, and a pond proteins using enzyme-linked immunosorbent assay banco and grassy rivers. In Adrar and Trarza, larvae of (ELISA), providing the first evidence that this species is An. pharoensis were caught in various mosquito develop- likely to play an important role in malaria transmission ment sites generally with clear or muddy and sometimes in the city. They also demonstrated the presence of An. slightly brackish water characterized by the presence of gambiae (s.s.), An. funestus, An. rufipes, An. pharoensis aquatic vegetation such as ponds, Tamourts,residual and An. arabiensis in Hodh Elgharbi region but were not pools, puddles and backwaters, rutted track, flooded able to incriminate any of them in malaria transmission in meadows on the Senegal River and Gueltas in the Adrar this region due to negative ELISA results although Hamon region. Breeding sites where larvae of An. pretoriensis et al. [20] found Plasmodium sporozoites in the salivary were collected in Hodh Elgharbi consisted of the affluent glands of two of 18 female An. gambiae collected in Hodh of permanent sources, with abundant vegetation and Elgharbi during October and November 1963 and re- much organic debris. Larvae of An. squamosus were found ported an overall sporozoite index of 0.45% (2/444) for all in grassy flats of cool or warm water, often muddy, study sites. Similar infection rate was reported by Pichon sometimes slightly brackish such as swamps, Tamourts, &Ouedraogo[35]inAn. gambiae specimens collected flooded meadows and streams. In Adrar, the breeding from different sites in southern Mauritania. site was a large Guelta. Specimens of An. domicola were recently reported by In Nouakchott, where An. arabiensis seems to be the Ouldabdallahi Moukah et al. [48] in Boghé (Brakna re- sole Anopheles species thriving in this arid and human- gion) and (Guidimagha region) located on the made environment, water bodies consisting of water dis- Senegal River. This species was already reported in charged from standpipes and household drinking water Barkedji and Kédougou in Senegal [49]. tanks served as An. arabiensis larval habitats [50, 51]. Environmental factors associated with anopheline lar- Using multivariate regression analyses, it was further val habitats and their types have not been extensively shown that salinity up to 0.1 g/l and shaded habitats studied in Mauritania. The available data were obtained were protective factors against high larvae density in from the works of Maffi [19], Hamon et al. [20] and breeding sites and that pH up to 7.61 was a risk factor Ould Ahmedou Salem et al. [50]. Larvae of An. rhode- for high larvae density in these breeding sites [50]. siensis were found in high density exclusively in the cold Studies on the insecticide susceptibility of anopheline and shaded water of springs in the sandstone massifs mosquitoes in Mauritania are limited. In 2005, Ba [44] Mint Mohamed Lemine et al. Parasites & Vectors (2017) 10:35 Page 8 of 13

tested the susceptibility to 0.75% permethrin and 0.05% Aedes aegypti aegypti, Ae. vittatus and Ae. caspius deltamethrin, of An. gambiae (s.l.)andAn. pharoensis from immature stages were isolated from diverse habitats Boghé (Brakna), (Trarza), Sélibaby (Guidimagha) and including abandoned containers, big canaries of drink- Aioun (Hodh Elgharbi). For permethrin, An. gambiae (s.l.) ing water, poultry water trough, household drinking specimens from all sites were sensitive. At Rosso and water tanks, rock holes and rain puddles, respectively Boghé, there was 100% mortality among An. pharoensis fe- [35, 51, 54]. Furthermore, it has been shown that Ae. males tested. For deltamethrin, only An. pharoensis speci- aegypti development sites in southern Mauritania mens from Rosso were tested. The applied concentration were closely related to the habits of different ethnic resulted in 100% mortality. groups regarding the mode of water storage. For instance, The genetic profile of insecticide resistance was re- canaries of drinking water used by the Soninke people cently assessed in An. gambiae (s.l.) populations in Hodh were the main larval development sites of the species in Elgharbi (Sahelian zone) and Nouakchott (Saharan zone) Guidimigha and part of Gorgol regions [35]. No data on [47]. Analysis of pyrethroid knockdown resistance (kdr) insecticide resistance in this species is currently available gene polymorphism showed the predominance of wild- for Mauritania. type kdr L1014 among An. arabiensis in the two regions. Both kdr point mutations (L1014S and L1014F) were found to co-exist in the mosquitoes examined. However, Culex spp. the most important finding in this study was the pres- A total of 18 Culex species were described in Mauritania ence of a high proportion of the east African mutation (Table 1). These are Cx. antennatus, Cx. decens, Cx. nea- (L1014S) among An. arabiensis captured in Nouakchott. vei, Cx. perfuscus, Cx. poicilipes, Cx. quinquefasciatus, This mutation which was initially observed only in East Cx. perexiguus, Cx. tigripes, Cx. ethiopicus,Cx. simpsoni, Africa [52], now appears to be invading West Africa Cx. pipiens, Cx. fatigans, Cx. univittatus, Cx. duttoni, [53]. None of the assessed mosquitoes showed mutations Cx. grahami, Cx. annulioris, Cx. nebulosus and Cx. tri- in the acetylcholinesterase resistance (ace-1) gene. taeniorhynchus [8, 9, 21, 23, 35, 41]. Apart from the malariometric survey of Hamon et al. [21] in which ten Aedes spp. Culex species were identified in different regions of Fourteen Aedes species were described in Mauritania Mauritania and that of Pichon and Ouedraogo [35] ex- (Table 1). The presence of Aedes spp. was first docu- ploring potential conditions for the emergence of YF ep- mented in the late 1960s with the reports of Ae. scato- idemics, where 16 Culex species have been described, all phagoides, Ae. metallicus and Ae. luteocephalus in Kaedi entomological investigations reporting the presence of (Gorgol) in the Senegal River valley, Ae. vittatus, Ae. ochra- Culex species were closely related to the epidemics of ceus and Ae. aegypti in the southernmost regions of Gorgol, RVF in Mauritania. Indeed, during their survey of 1998, Assaba, Guidimagha and Ae. hirsutus in the southeastern following the RVF outbreak in Hodh Elgharbi region regions of Hodh Elgharbi and Hodh Charghi [21, 35, 54, (south-eastern Mauritania), Nabeth et al. [41] using 55]. Aedes vexans, the chief enzootic vector subspecies of CDC light traps with CO2 set nearby temporary ground RVF, was collected from Trarza, Brakna, Assaba, Adrar and pools and CDC light traps without CO2 set in sheepfolds Hodh Elgharbi regions and Senegal using four different or cowsheds, captured Cx. antennatus, Cx. decens, Cx. methods: CDC light traps, animal baited traps, landing neavei, Cx. perfuscus, Cx. poicilipes and Cx. quinquefas- catches on human baits and aspiration inside human dwell- ciatus but they were not able to isolate RVF virus among ings [8, 9, 23, 44, 56]. Specimens of Ae. vexans and Ae. captured mosquitoes. However, entomological investiga- sudanensis were also captured in Tagant and Hodh Elgharbi tions conducted in 1998 and 1999 in Hodh Elgharbi regions, following the RVF outbreaks of 1998–1999 and where the same RVF outbreak occurred and the Tagant 2012 [8, 23]. Entomological surveys carried out in Senegal central region, Diallo et al. [8] captured Cx. poicilipes River valley, few years after the first documented RVF out- specimens naturally infected with RVF virus. During break that occurred in 1987 in southern Mauritania, sug- the following RVF outbreaks in 2003 which affected gested that Ae. vexans and probably Ae. ochraceus may be Trarza, Brakna and Assaba southern regions of involved in the transmission of this epizootic disease since Mauritania and in 2012 which occurred in the northern ten and three RVF virus strains were isolated from these Adrar region, Cx. poicilipes together with Cx. antennatus two species during the survey, respectively [3]. Recently, the were found positive with RVF viruses [9, 12]. Culex poici- presence of Ae. aegypti aegypti and Ae. caspius was reported lipes was already incriminated as RVF vector in Senegal for the first time in Nouakchott [51]. DF outbreaks occurred during an entomological survey undertaken to assess in 2015 in the city (Ministry of Health, unpublished data) the extent of virus circulation in this country follow- and specimens of Ae. aegypti have been regularly captured ing the re-emergence of the RVF virus in Hodh since that time (Mint Lekweiry, pers. comm.). Elgharbi region in 1998 [57]. Mint Mohamed Lemine et al. Parasites & Vectors (2017) 10:35 Page 9 of 13

Other Culicidae vectors in Africa, and its wide distribution in Mauritania Two Mansonia species, namely Ma. uniformis and Ma. agrees with the general distribution of the species in Africa africana, were reported to occur in Mauritania (Table 1). [59] and particularly in the neighboring country of Senegal Mansonia africana was first collected in Gorgol by [60]. Anopheles gambiae (s.s.), An. funestus and four Hamon et al. [21]. Its presence was recently confirmed secondary malaria vectors (An. coustani, An. ziemanni, by Faye et al. [9], but these authors prospected 11 local- An. pharoensis and An. wellcomei) were also reported, but ities in Trarza, Brakna and Assaba regions without stat- their role as malaria vectors in Mauritania has not been ing in which of them the specimens of Mansonia were established so far. collected. Mansonia uniformis was also collected either Culex poicilipes and Cx. antennatus were incriminated before 1970 or more recently either in the Saharan in the repeated RVF outbreaks and Aedes aegypti was (Adrar and Tagant) or the Sahelian (Hodh Charghi, Trarza probably responsible of the recent DF outbreaks occur- and Gorgol) regions of the country [9, 21, 23, 35]. Al- ring in Nouakchott in 2014 and 2015. However, at though females of both species were identified among bit- present, a definite proof linking these mosquito species ing mosquito populations in Mauritania, their medical to RVF and DF is yet to be established. importance has not yet been elucidated. Spatial and temporal distribution of the Culicidae fauna in Mauritania is heterogeneous. The southern Discussion Gorgol and Trarza, and central Tagant and Assaba re- This report updates available knowledge on mosquito gions of the country are the richest in species diversity biodiversity in Mauritania through an extensive review with 18, 17, 17 and 14 species over the 49 scored, re- of entomological findings gathered in the country from spectively. Mosquito biodiversity is much lower in the 1948 to 2016. Most of the reviewed literature dealt with northernmost regions. However, there are no or few data the inventory, distribution and ecology of the mosquito on the mosquito biodiversity from the southeastern fauna focusing on those of medical importance, particu- Hodh Charghi region and from most of the northern larly anopheline mosquitoes. While research carried out Saharan regions of the country. Because oases might before 1970 was limited and was often part of the mal- serve as “hubs” for human as well as livestock migration aria pre-elimination programme at that time, entomo- throughout the desert, entomological surveillance should logical research gained momentum at the beginning of be regularly implemented in these areas to explore the the twentieth century after the repeated outbreaks of risk for pathogen emergence. RVF of 1987 and 1998 in the south and southeastern re- According to Hamon et al. [20], the fauna of central gions of Mauritania where the disease became endemic and southern Mauritania is closely related to those of since that time [10]. Senegal, southern Mali and northern Sudan, while the Mosquito-transmitted diseases including malaria, RVF fauna of the northern Saharan region of Adrar is likely and DF have been reported, and for malaria, confirmed to have more affinity with the arid regions of Chad, to occur in Mauritania. Fever outbreaks that occurred in Somalia, Arabian Peninsula and North Africa. 2014 and 2015 in Nouakchott were initially suspected to The heterogeneity in the spatial and temporal distribu- be malaria infections, but diagnosis using the commer- tion of the Culicidae biodiversity in Mauritania observed cial SD Bioline Dengue NS1 Ag Rapid Test (Standard in the reviewed literature, could be explained, at least Diagnostics Inc., Gyeonggi-do, South Korea) confirmed partially, by the differences in the investigation periods the infection with DF virus (Ouldabdallahi Moukah, un- (dry season versus wet season), their short time period published data). They were later officially recognized by and occasional nature (most site were visited only once the Mauritanian Health officials and notified to the during an investigation and always after an epidemic) and WHO in 2015 together with the RVF outbreak that oc- the method with which mosquitoes were collected (light curred in Brakna region. traps, human baited trap, larval collection, PSC, etc.). Malaria is transmitted by species of the An. gambiae (s.l.) However, it could be assumed that at least for some complex, represented mainly by An. arabiensis. Its vectorial species, events of extinction or introduction have prob- capacity was recently demonstrated in Nouakchott and in ably occurred. For instance, while Hudleston [61] sug- the southern region of Assaba [22, 46, 47]. The presence of gested that mosquitoes of the An. gambiae (s.l.) complex An. arabiensis in Mauritania was first reported by the had a northern limit that passed through Boutilimit works of Hamon et al. [20] who suggested that the speci- (17°32′N) situated in the Saharo-Sahelian zone, An. mens of An. gambiae (s.l.) captured during their survey arabiensis has recently been reported further to the were most probably An. gambiae (species B), later known north, particularly in Nouakchott (18°32′N), the cap- as An. arabiensis [58], which generally occurs in more arid ital city [47] and Rachid (18°47′N) in the Tagant re- habitats than the other members of the complex. Anoph- gion [44]. Its presence in Nouakchott is probably the eles arabiensis is one of the three most efficient malaria cause of the establishment of malaria transmission in Mint Mohamed Lemine et al. Parasites & Vectors (2017) 10:35 Page 10 of 13

this city which was considered until the recent past as Moreover, intense human and livestock movements malaria-free [14, 15, 47]. Conversely, An. melas and An. occur annually in Mauritania. Human population move- gambiae (s.s.) have shrunk their distribution areas com- ments are mostly seasonal and occur mainly between pared to the 1960s. Indeed, after the construction of the Nouakchott and the established malaria endemic zones. anti-salt Diama dam in 1986, on the Senegal river, An. This population flux partly related to school vacation melas populations previously recorded in the localities of from July to the beginning of October had probably con- Richard Toll (15°41′W) and Tounguen (15°46′W) in tributed to the introduction of infectious diseases, par- Senegal and Mauritania, respectively [20, 36] have moved ticularly malaria, from the southern endemic regions to westward to Saint-Louis (16°28′W) near the Atlantic the northern non-endemic regions and possibly contrib- coast, where saltwater breeding-places are present [38]. uted to the spread of An. arabiensis into the capital city Anopheles gambiae (s.s.) has probably experienced a simi- [64]. The role of human population movements in the lar event but due, this time, to the establishment of ex- spread of communicable diseases such as malaria has treme arid conditions in central Mauritania after the long been recognized [65]. 1970–1990s drought. Livestock movements also occur throughout the year The recent discovery of Ae. aegypti in Nouakchott [51] within Mauritania and from Mauritania to the neighbor- probably resulted from the expansion of more southern, ing Sahelian countries of Senegal and Mali. Cattles, contemporaneous populations thriving in sub-Saharan small ruminants and camels are moved every year for Africa. However, due to their limited sampling, these au- grazing or sale, favoring virus circulation by introducing thors were not able to rule out direct invasion from Asia, viraemic animals from an infected area to a receptive through passive dispersal and human-assisted egg trans- one as it has been suggested during the RVF outbreaks portation by plane and ship owing to the homology of in Hodh Elgharbi and Adrar regions [10, 41]. DNA sequence of the tested specimens with the published Furthermore, the construction in 1986 of the Diama Ae. aegypti accessions from Vietnam and Thailand. anti-salt Dam across the Senegal River coincided with It has been reported that mosquito colonization/ the first RVF outbreak that occurred in 1987 in southern extinction process, population dynamics and vector cap- Mauritania and may have been its main contributing acity in a given area depend on several factors such as avail- cause [7]. Indeed, Fontenille et al. [66] proposed that ability and type of larval development sites, climate and flooding of the river bank of the Senegal River in 1987, environmental changes, human population density, in- following construction of the dam, resulted in the in- creased human travel and goods transport, and reduction crease of both mosquito and livestock densities and was of resources in the life-cycle of mosquitoes by interventions probably the cause of this epizootic. RVF virus was iso- [62]. In Mauritania, climate and environmental changes, lated, 6 years later, from Ae. vexans and Ae. ochraceus population and livestock movements, development of mosquitoes and from one healthy sheep, in Barkedji hydroagricultural projects, improvement of land transport area, located in the Sahelian Ferlo region of Senegal infrastructures, and unplanned urbanization are probably [3, 56] and in several localities in Senegal and themostrelevantfactorsinthis context. The degradation Mauritania simultaneously following the RVF outbreak of the climatic conditions, caused by prolonged droughts of 1998 in Hodh Elgharbi [57]. during 1970–1990s in the Sahel resulted in a latitudinal Unplanned urbanization due to rapid demographic shift of 100 mm isohyets for 100 km to the south between growth characterized by poor housing, lack of sanitation, the periods 1947–1969 and 1970–1985. In Mauritania, iso- development of urban agriculture and inadequate sur- hyet 100 mm is even down by more than 200 km reaching face water drainage is often cited as one of the major Nouakchott region [63]. Desertification phenomenon then factors that influence the epidemiology of malaria and that progressed southwards limiting the number and the lon- of other emerging diseases, such as DF, in Nouakchott gevity of aquatic habitats which probably affected the bio- [50, 51]. This rapid urbanization creates new larval habi- diversity and distribution of the Culicidae. tats and maintains the presence of both An. arabiensis However, epidemics of vector-borne diseases, even in and Ae. aegypti in the city. the northern Saharan parts of the country, remain a To increase knowledge on the diversity and bionomics threat to public health particularly after natural disasters of mosquitoes in Mauritania, particularly those of med- such as flooding caused by heavy rainfall. For instance, ical importance, it is important to extend entomological RVF outbreaks in 1998 and 2010 in the Hodh Elgharbi surveys to the unexplored southeastern region of Hodh (Saharo-Sahelian) and the Adrar (Saharan) regions oc- Charghi which is the most populated region in the curring after an exceptionally heavy rainfall resulted in country with 412,939 (12.2%) inhabitants in 2013 highly favorable conditions for colonization and subse- [25]. The region is also characterized by the presence quent proliferation of competent vectors such as Ae. of several permanent and semi-permanent wetlands vexans, Cx. poicilipes and Cx. antennatus [10, 23]. locally known as Tamourts. Mint Mohamed Lemine et al. Parasites & Vectors (2017) 10:35 Page 11 of 13

There is also a need to introduce more efficient and ac- Authors’ contributions curate techniques to collect and identify mosquito fauna. AMML, MAOL, MHE, KML, MSOAS and MOM were involved in the conception of the idea, and conducted the literature searches. KOB, INOB, In this context, the establishment of an identification CB, JFT, LB, HB, FS, OF and AOMSB reviewed and analyzed the documents, guide for larvae and adult female of common mosquitoes and participated in writing the final manuscript. All authors read and in Mauritania based on morphological criteria and/or mo- approved the final manuscript. lecular biology for species that are closely related such as Competing interests members of the An. gambiae (s.l.) complex is an urgent The authors declare that they have no competing interests. task. This effort should be sustained by the development of skills and capacity building in medical entomology Consent for publication where the number of researchers at present does not meet Not applicable. the needs of a vast country like Mauritania. As Mauritania moves towards malaria elimination by Ethics approval and consent to participate Not applicable. 2025, it will be necessary to continuously update the database of vector research and control by conducting Author details 1 ’ entomological surveillance and evaluation, as much of Unité de recherche Génomes et Milieux, Jeune Equipe Associée à l IRD (RI3M), Université de Nouakchott Al-Aasriya, Faculté des Sciences et the historical literature generated may not hold true at Techniques, Nouveau Campus Universitaire, Nouakchott BP 5026, Mauritania. present and in the future, as environmental landscapes 2Laboratoire d’Ecologie Vectorielle et Parasitaire, Faculté des Sciences et 3 continue to change. Within the context of malaria elim- Techniques, Université Cheikh Anta Diop, Dakar, Senegal. Institut Supérieur des Etudes technologiques, Rosso, Mauritania. 4Maladies Infectieuses et ination, the value of understanding the distribution and Vecteurs: Ecologie, Génétique, Evolution et Contrôle (MIVEGEC), Unité Mixte bionomics of An. arabiensis in Mauritania and its ability de Recherche IRD224-CNRS5290-Université de Montpellier, Institut de 5 to sustain malaria transmission cannot be understated. Recherche pour le Développement (IRD), Montpellier, France. Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE), UM 63, CNRS 7278, IRD 198, Inserm 1095, Faculté de Médecine La Timone, Conclusions Aix-Marseille Université, Marseille 13385, France. 6Unité Parasitologie et The present review highlights that knowledge about Entomologie, Département des Maladies Infectieuses, Institut de Recherche Biomédicale des Armées, Marseille, France. Mauritanian mosquito fauna is closely related to human health rather than the result of systematic entomological Received: 21 November 2016 Accepted: 10 January 2017 surveillance. The Culicidae fauna of Mauritania comprises 17 Anopheles spp., 14 Aedes spp., 18 Culex spp. and two References Mansonia spp. present in all ecological zones of Mauritania 1. Schaffner F, Angel G, Geoffroy B, Hervy JP, Rhaeim A. The mosquitoes of and including the major mosquito vectors of malaria, RVF Europe/Les moustiques d’Europe [computer program]. Montpellier: IRD and DF. Although this study represents important insights editions; 2001. 2. Becker N, Petric D, Zgomba M, Boase C, Madon M, Dahl C, et al. Mosquitoes into the mosquito diversity of Mauritania, 51 species and their control. London: Springer; 2010. p. 577. reported in this review are unlikely to be a complete 3. Fontenille D, Traoré-Lamizana M, Zeller H, Mondo M, Diallo M, Digoutte JP. inventory of the Mauritanian mosquito fauna probably Rift Valley fever in western Africa: isolations from Aedes mosquitoes during an interepizootic period. Am J Trop Med Hyg. 1995;52:403–4. because of the limited number of mosquito sampling 4. World Health Organization. A global brief on vector-borne diseases [WHO/ methods and the lack of knowledge on biodiversity in DCO/WHD/2014.1]. Geneva; 2014. southeastern and northern regions. A nationwide en- 5. Wilkerson RC, Linton Y-M, Fonseca DM, Schultz TR, Price DC, Strickman DA. Making mosquito taxonomy useful: a stable classification of tribe Aedini tomological field survey is necessary to update the list that balances utility with current knowledge of evolutionary relationships. of mosquito species and establish an identification PLoS One. 2015;10:e0133602. guide for both adult females and larval stages particu- 6. Freitas LA, Russo CAM, Voloch CM, Mutaquiha OCF, Marques LP. Schrago CG. Diversification of the genus Anopheles and a Neotropical clade from the larly for those of medical relevance. late Cretaceous. PLoS One. 2015;10(8):e0134462. 7. Digoutte JP, Peters CJ. General aspects of the 1987 Rift Valley fever Abbreviations epidemic in Mauritania. Res Virol. 1989;140:27–30. (s.l.): sensu lato;(s.s.): sensu stricto; Ace-1: acetylcholinesterase resistance gene; 8. Diallo M, Nabeth P, Ba K, Sall AA, Ba Y, Mondo M, et al. Mosquito vectors of CDC: Centers for Disease Control; DF: dengue fever; ELISA: enzyme-linked the 1998–1999 outbreak of Rift Valley fever and other arboviruses (Bagaza, immunosorbent assay; kdr: knockdown resistance; PSC: pyrethrum space-spray Sanar, Wesselsbron and West Nile) in Mauritania and Senegal. Med Vet catch; RVF: Rift Valley fever; WHO: World Health Organization; YF: yellow fever Entomol. 2005;19:119–26. 9. Faye O, Diallo M, Diop D, Bezeid OE, Ba H, Niang M, et al. Rift Valley fever Acknowledgements outbreak with east-central African virus lineage in Mauritania, 2003. Emerg We thank Dr Ould El Mamy Bezeid from the National Center of Veterinary Infect Dis. 2007;13:1016–23. Researches for his help. 10. Ould El Mamy AB, Ould Baba M, Barry Y, Isselmou K, Dia ML, Ba H, et al. Unexpected Rift Valley fever outbreak, northern Mauritania. Emerg Infect Funding Dis. 2011;17:1894–96. This work was published with the support of Institut de Recherche pour le 11. Caminade C, Ndione JA, Diallo M, MacLeod DA, Faye O, Ba Y, et al. Rift Développement (IRD) and Expertise France (Initiative 5%). Valley fever outbreaks in Mauritania and related environmental conditions. Inter J Environ Res Pub Health. 2014;11:903–18. Availability of data and materials 12. Faye O, Ba H, Ba Y, Freire CCM, Faye O, Ndiaye O, et al. Reemergence of Rift Not applicable. Valley fever, Mauritania. Emerg Infect Dis. 2014;20:300–3. Mint Mohamed Lemine et al. 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